The number 5 was assigned in 1924. At the time, all BMT Culver Line trains used the elevatedBMT Fifth Avenue Line, running over the Brooklyn Bridge to Park Row. Rush-hour trains made no stops between 36th Street and Atlantic Avenue (both directions in morning rush hour, southbound only in afternoon rush hour).

Subway trains started to run on the Culver Line on May 30, 1931, when the Nassau Street Loop was completed. These trains used the south half of the Nassau Loop, ending at Chambers Street. During rush hours and Saturday mornings, they used the full loop, entering Manhattan via the Manhattan Bridge and leaving via the Montague Street Tunnel. These trains only ran to Kings Highway on the Brooklyn end. Rush hour trains ran express on the BMT Fourth Avenue Line; trains operating in the reverse-peak direction ran express between Ninth Avenue and Kings Highway. Elevated service was cut back to Ninth Avenue, except during rush hours, when it was extended to Coney Island (and continued to run express on the Fifth Avenue Line, though both directions during both rush hours).

The BMT Fifth Avenue Line was closed on May 31, 1940, and from that time all Culver trains used the subway.

On October 30, 1954, the south part of the Culver Line was connected to the IND South Brooklyn Line, and BMT Culver trains were truncated to Ditmas Avenue, where there was a transfer to IND trains to Coney Island. Some Culver trains continued to run into Manhattan until 1959, when they were all truncated to a shuttle between Ninth Avenue and Ditmas Avenue.

This shuttle, assigned the label SS in 1960, last ran on May 10, 1975. The elevated trestle along with the 13th Avenue and Fort Hamilton Parkway stations stood abandoned until finally being demolished in the mid-1980s. The only remnants of the Culver Shuttle are the lower platforms and tracks at Ninth Avenue and a section of the trestle that is attached to the Coney Island bound platform at Ditmas Avenue on the Culver Line. The right of way has been sold, as houses have been built on the old right of way near the Ditmas Avenue station. After the shuttle was discontinued, new signs were hung stating what passengers had to do since the shuttle stopped running. A sign like this may have read:

Culver Shuttle service discontinued
Cross over to other platform
Ride one stop to Church Av
for B-35 bus transfer